Brachiopods: another piece in the puzzle of eye evolution

i-e88a953e59c2ce6c5e2ac4568c7f0c36-rb.png

About 600 million years ago, or a little more, there was a population of small wormlike creatures that were the forebears of all modern bilaterian animals. They were small, soft-bodied, and simple, not much more than a jellyfish in structure, and they lived by crawling sluglike over the soft muck of the sea bottom. We have no fossils of them, and no direct picture of their form, but we know a surprising amount about them because we can infer the nature of their genes.

These animals would have been the predecessors of flies and squid, cats and starfish, and what we can do is look at the genes that these diverse modern animals have, and those that are held in common we all inherited together from that distant ancestor. So we know that flies and cats both have hearts that are initiated in early development by the same genes, nkx2.5 and tinman, and infer that our common ancestor had a heart induced by those genes…and that it was only a simple muscular tube. We know that modern animals all have a body plan demarcated by expression of Hox genes, containing muscles expressing myoD, so it’s reasonable to deduce that our last common ancestor had a muscular and longitudinally patterned body. And all of us have anterior eyes demarcated by early expression of pax6, as did our ancient many-times-great grandparent worm.

i-273ccf6ddad17af1bbd4674e0fbc722e-matrix.jpeg

We do not have fossils of these small, soft organisms, but that’s no obstacle to picturing them. You just have to see the world like a modern molecular or developmental biologist. One of the graphical conceits of the Matrix movies was that the hero could see the hidden mathematical structure of the world, which was visualized as green streams of symbols flowing over everything. We aspire to the same understanding of the structure of life, only what we see are patterns of genetic circuity, shared modules that are whirring away throughout development to produce the forms we see with our eyes; and also, unfortunately, we currently only see these patterns spottily and murkily. There is no developmental biologist with the power of Neo yet, but give us a few decades.

There’s another thing we know about these ancient ancestors: they had two kinds of eyes. ciliary and rhabomeric. Your eyes contain ciliary photoreceptors; they have a particular cellular structure, and they use a recognizable form of opsin. A squid has a distinctly different kind of photoreceptor, called rhabdomeric, with a different cell structure and a different form of opsin. We humans also have some rhabdomeric receptors tucked away in our retinas, while invertebrates have ciliary receptors as well, so we know the common ancestor had both.

Now this ancestral population eventually split into two great tribes, the protostomes, which includes squid and flies, and the deuterostomes, which includes cats and starfish. It should be an obvious indication of the general state of that ancestor that it represents all that those four diverse animals have in common. It also tells us that while that ancestor had eyes, they were almost certainly very simple, and could have been nothing more than a patch of light-sensitive cells, or perhaps even single cells, as we see in some larval eyes.

What we think happened at this division is that both tribes took the primitive eyes and specialized them independently. Each group evolved under similar constraints: they needed directionally-sensitive eyes that could tell what direction a source of illumination was coming from (and these would eventually form true image-forming eyes), and they also needed sensors to detect general light levels — is it day or night, are we in the open or under a rock? Think of it like a camera system: there is a part that gets all the attention, the lens and image-forming chip, but there’s also a light meter that senses ambient light levels.

The two tribes made different choices, though. The protostomes pulled the rhabdomeric photoreceptor out of their toolbox, and used that to make the camera; they used the ciliary photoreceptor to make their light meter. The deuterostomes (actually, just us chordates) instead used the ciliary photoreceptor for their camera, and the rhabdomeric photoreceptor for the light meter. It’s the same ancestral toolkit, but we’ve just specialized in different ways.

At least, that’s the general model we’ve been exploring. A new discovery at the Kewalo Marine Laboratory, one of the premiere labs for evo-devo research, has made the interpretation a little more complex.

That discovery is that brachiopod larvae, which are protostomes, have been found to have directionally sensitive eyes…which are ciliary. A protostome should have directionally sensitive eyes that are rhabdomeric. How interesting!

i-d60159d94316ec8d38e4c091e84a429f-brachiopodeyes.jpeg
Brightfield microscopy of a Terebratalia transversa larva, with red eye spots visible in the apical lobe (black arrows). (A) Dorsal view. (B) Lateral view.

In addition to being ciliary in structure, these eyes express ciliary opsin. They are also true cerebral eyes, also expressing pax6 and having a nervous connection to the central nervous system.

Notice what is going on here: a protostome is building a camera, and unlike all the other protostomes we’ve observed, it’s pulled a ciliary photoreceptor out of its pocket to make it. This is a surprise, but it doesn’t upset any theories too much — it just means we need to explore a couple of alternative explanations. We don’t have answers to resolve these hypotheses yet — we need more data and experiments — but it’ll be fun to watch the work roll onward.

One explanation is illustrated in A, below. The initial animal state was to build directional, cerebral eyes using rhabdomeric photoreceptors. The vertebrates are oddballs who swapped in ciliary receptors instead, while these larval eyes in brachiopods are major peculiarities, an evolutionary novelty which resembles a cerebral eye, but is actually non-homologous. This seems unlikely to me; there are multiple elements of the eye circuitry at work in these eyes, and if they’re using the same gene circuitry, we ought to recognize them as homologous at the molecular level…the only one that counts.

The second explanation in B is that all of these cerebral eyes are homologous, but that the receptor type is more plastic than we thought — it’s relatively easy to switch on the ciliary module vs. the rhabodmeric module, so we would expect to see multiple flip-flops in the evolutionary record.

If we accept that it’s easy to switch receptor type, though, then why assume that the last common ancestor had a directional, cerebral eye that was rhabdomeric? It could have been ciliary, which is also a more parsimonious explanation, because it requires only one switch of types in the protostomes, shown in C.

i-ce7a3df55993c986b97d516e84e9041e-models-thumb-400x141-62593.jpeg
(Click for larger image)
Alternative hypothesis on the evolution of photoreceptor deployment in cerebral eyes. Schematic representation of three hypotheses accounting for the deployment of ciliary photoreceptors in the cerebral eyes of Terebratalia and vertebrates, versus rhabdomeric photoreceptors in Platynereis and other protostomes. (A) Deployment of rhabdomeric photoreceptors as the ancestral state in cerebral eyes, with the larval eyes of Terebratalia, containing ciliary photoreceptors, representing an evolutionary novelty. The deployment of ciliary photoreceptors is the result of a substitution (with ciliary photoreceptors having replaced rhabdomeric photoreceptors in the cerebral eyes) early in the chordate lineage. (B) Larval eyes in Terebratalia are homologous to the cerebral eyes in other protostomes, but ciliary photoreceptors have been substituted for rhabdomeric photoreceptors, as in the vertebrates. (C) Ciliary photoreceptors in cerebral eyes represent the ancestral condition, inherited by Terebratalia and vertebrates. Deployment of rhabdomeric photoreceptors in the cerebral eyes of Platynereis and other protostomes are the result of substitution events.

Whichever hypothesis pans out, though, the important message is that photoreceptor type is a more evolutionarily labile choice than previously thought. What I want to see is more research into photoreceptor development in more exotic invertebrates — that’s where we’ll learn more about our evolutionary history.

I have to mention a couple of other cool features of this paper. If you ever want to see a minimalist directional eye, here it is: the larval eye sensor of brachiopods consists of two cells, a lens cell that actually does the job of light detection, and a pigment cell that acts as a shade, preventing light from one direction from striking the lens cell. That’s all it takes.

i-b1738b6556ff1a04b804d4e4f22e11ce-2celleye.jpeg

I lied! That isn’t a minimal directional eye at all: here it is.

i-855bd089740480150447e707ace1fd5f-gastrula.jpeg

This rather blew my mind. The brachiopod gastrula senses light. The figure above is of a very early stage in development, when the organism is little more than a couple of sheets of cells with no organs at all, only tisses in the process of forming up into rough structures. It definitely has no brain, no nervous tissue at all, and no eyes…and there it is, that dark blue smear is a region selectively expressing ciliary opsin as if it were a retina. Furthermore, when tested behaviorally (mind blown again…behavior, in a gastrula), populations in a light box show a statistical tendency to drift into the light. Presumably, light stimulation of the opsin is coupled to the activity of cilia used for motility in the outer epithelium of the embryo.

Amazing. It suggests how eyes evolved in multicellular organisms, as well — initially, it was just localized general expression of light-sensitive molecules coupled directly to motors in the skin, no brain required.

Passamaneck Y, Furchheim N, Hejnol A, Martindale MQ, Lüter C (2011) Ciliary photoreceptors in the cerebral eyes of a protostome larva. EvoDevo, 2:6.

Soon to appear on a thousand herpetologist’s doors

xkcd digs into cladistics.

i-46b6ffb1cd5ac885a49421a7b2b27cde-herp1.jpeg i-4b78d9bd9df39c74b9c64683ce641f65-herp2.jpeg

Unfortunately, his cladogram is wrong. Mammals should also be a subset of the reptiles, so the herpetologists should be demanding that all other amniotes be absorbed into their more inclusive field of tetrapod biology.

At least, until the ichthyologists show up and point out that we’re all just weird dry land-walking fish.

Just to clear this up, I hope, here’s a modified version of a cladistic diagram to show what herps are:

i-b99daaa4d7677203e77e4656291ebc91-herps.jpg

So if you want to avoid the sins of polyphyly or paraphyly, you must include birds and mammals in the herps. Of course, the alternative is to not care about the abstractions, and recognize that there are plenty of people already specializing in mammals and birds, so someone has to pay attention to all the otherwise neglected classes.

How to tell you’re arguing with an idiot

There are some useful tells. My favorite has the been the classic quotemine, where creationists quote one sentence of Darwin’s — “To suppose that the eye, with all its inimitable contrivances for adjusting the focus to different distances, for admitting different amounts of light, and for the correction of spherical and chromatic aberration, could have been formed by natural selection, seems, I freely confess, absurd in the highest possible degree” — to claim that Darwin was stumped by the evolution of the eye. As everyone who has read the Origin knows, what he was doing there was setting up a rhetorical question, which he then followed by three pages of detailed description of exactly how such an eye could have evolved. When you hear some creationist say “absurd in the highest possible degree,” you know right away that they haven’t read the book.

There’s another great example, though, that’s an even better demonstration of your opponent’s illiteracy. That is when someone cites The Selfish Gene and then goes on to rail against the horrors of evilution and the way it encourages people to be righteous bastards who kill and steal and rape their way to dominance. They haven’t read the book! All they’ve done is scanned a three word title and leapt to a series of absurd conclusions! (Yeah, Mary Midgley, I’m givin’ you the squinky eye.)

Ken MacLeod exposes the inanity of this claim in some detail. It really is astoundingly common for people to expound on how Richard Dawkins was arguing for the rightness of Thatcherism or whatever reactionary conservative policy they think he was endorsing, and get the whole story completely wrong — it really is a great tell. Unfortunately, it seems to expose left wing idiocy more than that of the right, but only because I think the righties make the same invalid assumptions, but since they like that error, they tend not to criticize.

Evolve a car

Looking for a nice demonstration of genetic algorithms? Here’s a simulation that takes randomized connected collections of polygons and wheels and scores them for their ability to traverse a rugged 2D landscape. I tried it last night, and it gave me an assortment of very bad vehicles: for example, a lot of them were just polygonal lumps that fell flat and sat there, while some had an odd wheel here and there, but also pointy bits that acted as brakes, or wheels that pointed upward at the sky and did nothing at all. So I just left it running and went to bed.

This morning, I’ve got strange vehicles running races on my computer screen. Unsurprising, but still kind of cool.

I have annoyed Jesse Bering

That’s what I do, after all. I strongly criticized his uncritical analysis of a set of rape-related evolutionary psychology studies, and now he responds with a rebuttal. It’s not a very good rebuttal, but I highly recommend his second paragraph in which he lists a good collection of links to several people who also ripped into his article. That part is excellent!

But then let’s get into the part where he argues with me.

P.Z. Myers is not, of course, the undisputed public ambassador of his discipline (although I’ve no doubt he sees himself as such), and by no means does the following apply to all biologists, or even all those who are critical of evolutionary psychology. But Myers’ affect-laden views regarding evolutionary psychology do represent those of at least a significant and vocal minority.

Not an auspicious start to accuse me of regarding myself as “the undisputed public ambassador of” biology, which certainly isn’t the case. This is a blog written by a professor in a small town in rural Minnesota. I’m kind of aware of exactly what it is, and lack the airs Bering wants to assign to me. But then, this isn’t surprising, since most of his following arguments rely on telling me what I intended, and he also gets that wrong. Except this little bit, where he does get the overall objections right.

Critics are particularly irritated by the fact that evolutionary psychologists do not test for genetic inheritance of the very traits they argue are adaptive but instead rely on behavioral or self-report measures to evaluate their theories. They also believe that evolutionary psychologists take too many story-telling liberties in reconstructing the ancestral past, since we can never know for certain what life was like hundreds of thousands of years ago, when such traits would have, theoretically, been favored by natural selection. (This is a point also stressed by Rennie in his critique of my Slate essay.) According to Myers, the whole messy endeavor, therefore, “is a teetering pyramid of stacked ‘couldas’ and guesses that it woulda had an influence on evolution.”

This is actually a reasonable summary of my general disagreements with evolutionary psychology. They are quite fond of inventing evolutionary stories about phenomena that don’t even have an iota of evidence for being genetic, and can come up with truly awesome causal accounts for even the most trivial observations.

He picks out one of my objections to argue why the evolutionary psychology crowd can’t do one of the experiments I didn’t suggest doing, which is a little odd, but OK.

In his post, Myers uses my discussion of the evolution of the human penis as a prime example of the sloppy work being done in the study of evolution and human behavior. He pillories psychologist Gordon Gallup’s famous “dildo study,” which suggests that the distinctive mushroom-capped shape of the penis might serve to scoop a competitor’s semen out of the vagina. (I described this work at long, intimate length in two prior articles in Scientific American.) Myers calls this penis study “tripe” because Gallup and his colleagues failed to show how variations in penis shape within a population–and variations in how the penis is used for coital thrusting–directly affect fertilization rates. Instead, the researchers relied on dildos of different designs, surveys of college students’ detailing their sexual behaviors, and a batch of artificial semen.

Now, I can only assume that Myers has not had to face a university human-research ethics committee in the past several decades. If he had, he would realize that his suggested empirical approach would be unilaterally rejected by these conservative bureaucratic gatekeepers. Does Myers really believe that these seasoned investigators wouldn’t rather have done the full experiment he describes–if only they lived in a less prudish and libellous university world? The fact of the matter is that research psychologists studying human sexuality are hamstrung by necessary ethical constraints when designing their studies. Perhaps Myers would be happy enough to allow investigators into his bedroom to examine the precise depth and vigor to which he plunges into his wife’s vaginal canal after they’ve been separated for a week, but most couples would be a tad more reticent. Gallup’s dildo study, and his related work on penis evolution, offered an ingenious–ingenious–way to get around some very real practical and ethical limitations. Is it perfect? No. Again, the perfect study, conceptually speaking, is often the least ethical one, at least as deemed by research ethics committees. But was it driven by clear, testable, evolutionary hypotheses? Yes. And it offered useful information that was otherwise unknown.

Telling me that they can’t do an experiment that I didn’t suggest doing doesn’t really undermine anything I said. I’m perfectly aware of the ethical limitations of human research, which is one reason why I work on animal models. The problem is that what I actually offered as shortcomings of the work wasn’t their failure to wire up my genitals, but this:

They don’t have any evidence that this behavior actually affects the fertilization rate of one partner’s sperm over another, they don’t have any indication of morphological differences in human populations that make some individuals better semen-scoopers, they don’t have any evidence that this behavior has had a differential effect in human history.

Those are the criteria I would expect to see met in order to discuss this issue as an evolutionary problem; what Bering’s sources were studying were mechanical and physiological aspects of some plumbing (which can be interesting!), and then tacking on unwarranted conclusions about evolutionary history. In fact, I don’t see how Bering’s strange and unexecutable experiment of logging the details of my personal sexual behavior would even touch my evolutionary objections.

He also skips over another relevant point I emphasized. I read the research papers he cited. These were studies that had him “riveted, and convinced”, but when I looked at, for instance, the study that found an increase in women’s handgrip strength during ovulation, the paper itself mentioned that there were many other studies that showed no variation in strength over the menstrual cycle. Which is it? Do you just pick the result that favors your interpretation?

Jerry Coyne has a summary of reactions, too, and mentions several instances where the papers aren’t as clear in their support of the evo-psych hypotheses as is claimed. These are very noisy data that sometimes support and sometimes contradict their claims, and it seems that whatever result they pluck out of the mess, it’s always in support of some purported evolutionarily significant effect on behavior or physiology.

As I said in my previous article, I think the general claim of evolutionary psychology, that our current behavior has been shaped by our biological history, is true. I think much of the research in the field is damaging to their thesis, though, not because it demonstrates the opposite, but because it flits over tiny details, like monthly variations in how a woman moves her hips or how she feels about men, and pretends that they’re all examples of the power of natural selection in sculpting a genome that encodes every pelvic wobble and every nerve impulse. It’s become a kind of modern ornithomancy, where each dip and swirl and change in direction of a flight of birds is interpreted as directly connected to the fate of nations. I remain unconvinced.

The evolution of rape?

There are days when I simply cannot bear the entire field of evolutionary psychology: it’s so deeply tainted with bad research and a lack of rigor. And that makes me uncomfortable, because the fundamental premise, that our behaviors are a product of our history, is self-evidently true. It’s just that researchers in this field couple an acceptance of that premise to a deep assumption of adaptive teleology, the very thing that they should be evaluating, and produce some of the most awesomely trivial drivel.

I’ve just finished reading an article titled “Darwin’s Rape Whistle: Have women evolved to protect themselves from sexual assault?“, and it’s everything I despise about evolutionary psychology. It’s nothing but sloppy thinking and poor science propped up by a conviction that plausibility is sufficient support for certainty.

I could fulminate for a few hours over this crap, but fortunately Jerry Coyne has calmly criticized the mess, so I’ll just make a few points.

The story is that women have evolved specific adaptive responses to the threat of rape. In support of this conclusion, the author cites various studies that claim to show that ovulating women show stronger handgrip strength (the better to fight off men who want to assault their eggs with sperm), that ovulating women are more suspicious of men, that ovulating women are more likely to avoid risky behaviors, and that ovulating white women become more fearful of black men. I’m unimpressed. All of the studies involve small numbers, typically of college students at American universities (and even more narrowly, of psychology students), and all involve responses to highly subjective stimuli. When you examine the literature cited in these papers, you discover that different investigators get different results — the handgrip study even admits up front that there are conflicting results, with other papers finding no differences in performance across the menstrual cycle. None test anything to do with inheritance, none try (or even can) look at the genetic basis of the behaviors they are studying. Yet somehow evolutionary psychologists conclude that “women may have been selected during human evolution to behave in ways that reduce the likelihood of conception as a consequence of rape.”

Another way to look at it is that they are hypothesizing that women are more likely to behave in ways that invite physical attack and brutal abuse when they aren’t ovulating. That is a remarkable assertion. It also carries the strange implication that the consequences of rape can be measured by the likelihood of immediate fertilization, rather than by the toll of physical injury and emotional trauma, a peculiar thing for psychologists to neglect. Wouldn’t it make more sense to have a general hypothesis that people, men and women, who can avoid violence at any time in their life, are more likely to be reproductively successful and thereby pass on their genes to subsequent generations? That’s all they’re saying, essentially, and the straining to sex it up by tying globally useful behaviors to reproductive cycles is unconvincing.

And of course they’re looking at culturally conditioned behaviors and responses in a narrow subset of the modern human population. How likely is it that a close-knit tribe of 30 hunter-gatherers has a serious problem with rape? Wouldn’t the nature of the culture be of far greater effect in determining the frequency of pregnancy due to rape than variations in handgrip strength or variations in fearfulness in women?

Then many of the studies that are described with such enthusiastic certainty as having definitive results turn out to be subjective, pointless messes. For instance, Jesse Bering concludes that sperm competition had to have been a very significant factor in our profligately promiscuous ancestors, and that the shape of the human penis has been selected specifically for a function in extracting competitor’s sperm from the vaginal canal. Unfortunately, when you look at the actual research cited for this semen-scooping function, it’s underwhelming.

To test this hypothesis, Gallup, Burch, Zappieri, Parvez, Stockwell, and Davis (2003) simulated sexual encounters using artificial models and measured the magnitude of artificial semen displacement as a function of phallus configuration, depth of thrusting, and semen viscosity. The displacement of simulated semen was robust across different prosthetic phalluses, different artificial vaginas, different semen recipes, and different semen viscosities. The magnitude of semen displacement was directly proportional to the depth of thrusting and inversely proportional to semen viscosity. By manipulating different characteristics of artificial phalluses, the coronal ridge and frenulum were identified as key
morphological features involved in mediating the semen displacement effect.

Under conditions that raise the possibility of females engaging in extra-pair copulations (i.e., periods of separation from their partner, allegations of female infidelity), Gallup et al. (2003) also found that males appear to modify the use of their penis in ways that are consistent with the displacement hypothesis. Based on anonymous surveys of over 600 college students, many sexually active males and females reported deeper and more vigorous thrusting when in-pair sex occurred
under conditions related to an increased likelihood of female infidelity.

Got that? They have studies that show that a piston displaces fluids more effectively in proportion to the depth of movement, and that college students report that when they suspect their partner of infidelity, they screw harder. They don’t have any evidence that this behavior actually affects the fertilization rate of one partner’s sperm over another, they don’t have any indication of morphological differences in human populations that make some individuals better semen-scoopers, they don’t have any evidence that this behavior has had a differential effect in human history. It’s all a teetering pyramid of stacked “couldas” and guesses that it woulda had an influence on evolution, if there were any variation and heritable factors involved in this function.

Whenever I see this kind of tripe from evolutionary psychologists, I reflexively reach for a counter-example, and recommend that everyone read one excellent book: The Case of the Female Orgasm: Bias in the Science of Evolution, by Elisabeth Lloyd. It’s a wonderful example of solid, rigorous, scientific thinking about an evolutionary phenomenon. Lloyd analyzes a score of adaptive just-so stories about the female orgasm, carefully scrutinizing the evidence for each, and discovers that the substance is wanting. Too often investigators start with the assumption that a feature absolutely must have been selected for, or it wouldn’t be there, and then contrive elaborate rationalizations for processes that could have favored its preservation in our ancestry…and the aura of plausibility is then sufficient to conclude that it must be so, even in the absence of any supporting evidence, and sometimes even in the face of contradictory evidence.

I should reread it now — if nothing else, to wash that nasty tincture of evolutionary psychology out of my brain.

Evolution: The Story of Life on Earth

Have you got kids? Are you tangentially related to any young people? Are you young yourself? Do you know anyone who just likes a good story and interesting science?

Well, then, I’m sorry, but reading this article will cost you $12.89. Jay Hosler has a new book out (illustrated by Kevin Cannon and Zander Cannon), Evolution: The Story of Life on Earth(amzn/b&n/abe/pwll), and I’m afraid it’s going to be required reading for everyone, and you’re also all probably going to end up buying multiple copies for gifts.

Really, it’s that good. It’s a comic book about aliens from Glargalia explaining the history of life on earth to young Prince Floorsh by going over the fundamental concepts and hitting a few of the details. It’s entertaining and fun, and sneakily informative.

If you don’t simply trust me, check out the extensive excerpts at the NCSE and at Scientific American.

Hey, and if you don’t like comic books, don’t know any young people, and don’t want to read it yourself, buy a copy anyway and give it to your local library. For America.

The new phrenology

Morphological variation is important, it’s interesting…and it’s also common. It’s one of my major scientific interests — I’m actually beginning a new research project this spring with a student and I doing some pilot experiments to evaluate variation in wild populations here in western Minnesota, so I’m even putting my research time where my mouth is in this case. There has been some wonderful prior work in this area: I’ll just mention a paper by Shubin, Wake, and Crawford from 1995 that examined limb skeletal morphology in a population of newts, and found notable variation in the wrist elements — only about 70% had the canonical organization of limb bones.

i-1c9f04cedab9162d0f515173b1984313-taricha.jpeg

i-d03621754561d5ba17e77b0065cad98a-aorta.jpg

I’ve also mentioned the fascinating variation in the morphology of the human aorta. Anatomy textbooks lay out the most common patterns, but anyone who has taught the subject knows that once you start dissecting, you always find surprises, and that’s OK: variation is the raw material of evolution, so it’s what we expect.

The interesting part is trying to figure out what causes these differences in populations. We can sort explanations into three major categories.

  1. Genetic variation. It may be the the reason different morphs are found is that they carry different alleles for traits that influence the developmental processes that build features of the organism. Consider family resemblances, for instance: your nose or chin might be a recognizable family trait that you’ve inherited from one of your parents, and may pass on to your children.

  2. Environmental variation. The specific pattern of expression of some features may be modified by environmental factors. In larval zebrafish, for instance, the final number of somites varies to a small degree, and can be biased by the temperature at which they are raised. They’re also susceptible to heat shock, which can generate segmentation abnormalities.

  3. Developmental noise. Sometimes, maybe often, the specific details of formation of a structure may not be precisely determined — they wobble a bit. The limb variation Shubin and others saw, for example, was almost entirely asymmetric, so it’s not likely to have been either genetic or environmental. They were just a consequence of common micro-accidents that almost certainly had no significant effect on limb function.

When I see variation, the first question that pops into my head is which of the above three categories it falls into. The second question is usually whether the variation does anything — while some may have consequences on physiology or movement or sexual attractiveness, for instance, others may really be entirely neutral, representing equivalent functional alternatives. Those are the interesting questions that begin inquiry; observing variation is just a starting point for asking good questions about causes and effects, if any.

I bring up this subject as a roundabout introduction to why I find myself extremely peeved by a recent bit of nonsense in the press: the claim that liberal and conservative brains have a different organization, with conservatives having larger amygdalas (“associated with anxiety and emotions”) and liberals having a larger anterior cingulate (“associated with courage and looking on the bright side of life”).

Gag.

I don’t deny the existence of anatomical variation in the brain — I expect it (see above). I don’t question the ability of the technique, using MRI, to measure the dimensions of internal structures. I even think these kinds of structural variations warrant more investigation — I think there are great opportunities for future research to use these tools to look for potential effects of these differences.

What offends me are a number of things. One is that the interesting questions are ignored. Is this variation genetic, environmental, or simply a product of slop in the system? Does it actually have behavioral consequences? The authors babble about some correlation with political preferences, but they have no theoretical basis for drawing that conclusion, and they can’t even address the direction of causality (which they assume is there) — does having a larger amygdala make you conservative, or does exercising conservative views enlarge the amygdala?

I really resent the foolish categorization of the functions of these brain regions. Courage is an awfully complex aspect of personality and emotion and cognition to simply assign to one part of the brain; I don’t even know how to define “courage” neurologically. Are we still playing the magical game of phrenology here? This is not how the brain works!

Furthermore, they’re picking on a complex phenomenon and making it binary. Aren’t there more than one way each to be a conservative or a liberal? Aren’t these complicated human beings who vary in an incredibly large number of dimensions, too many to be simply lumped into one of two types on the basis of a simple survey?

This is bad science in a number of other ways. It was done at the request of a British radio channel; they essentially wanted some easily digestible fluff for their audience. The investigator, Geraint Rees, has published quite a few papers in credible journals — is this really the kind of dubious pop-culture crap he wants to be known for? The data is also feeble, based on scans of two politicians, followed by digging through scans and questionnaires filled out by 90 students. This is blatant statistical fishing, dredging a complex data set for correlations after the fact. I really, really, really detest studies like that.

And here’s a remarkable thing: I haven’t seen the actual data yet. I don’t know how much variation there is, or how weak or strong their correlations are. It’s because I can’t. This work was done as a radio stunt, is now being touted in various other media, and the paper hasn’t been published yet. It’ll be out sometime this year, in an unnamed journal.

We were just discussing the so-called “decline effect”, to which my answer was that science is hard, it takes rigor and discipline to overcome errors in analysis and interpretation, and sometimes marginal effects take a great deal of time to be resolved one way or the other…and in particular, sometimes these marginal results get over-inflated into undeserved significance, and it takes years to clear up the record.

This study is a perfect example of the kind of inept methodology and lazy fishing for data instead of information that is the root of the real problem. Science is fine, but sometimes gets obscured by the kind of noise this paper is promoting.

I have to acknowledge that I ran across this tripe via Blue Girl, who dismisses it as “sweeping proclamations about the neurophysiological superiority of the liberal brain”, and Amanda Marcotte, who rejects it because “This kind of thing is inexcusable, both from a fact-based perspective and because the implication is that people who are conservative can’t help themselves.” Exactly right. This kind of story is complete crap from the premise to the data to the interpretations.

Why there are no missing links

This topic came up earlier this week: creationists are always yammering about the “missing link” and how it’s missing and therefore evolution is unsupported by the evidence. It’s total nonsense, since evolution doesn’t predict a “missing link”, but it seemed worthwhile to explain why, since there was a recent publication of some exciting data that demonstrates the real complexity of the situation.

Jim Foley and John Hawks and Carl Zimmer have written up the story of the Denisovans. To summarize, another group of Pleistocene humans have been sequenced, called the Denisovans — their identity is murky, as they’ve only been recognized by a few bones, but the results show that they were genetically distinct from both modern humans and Neandertals, another Pleistocene group that has been sequenced. Like the Neandertal story, in which some Neandertal genes (less than 5%) were introduced into some modern human (European and Asian) populations, what we know about the Denisovans is that some of their genes, about 5%, also spread into a subset of modern human populations, in this case the Melanesians.

That’s awesome stuff. There are all these splintered bits of ancestry that come together in complex ways to produce the human species, and that’s why there is no missing link. Many people have this false notion that our evolution was a matter of a panmictic gemisch of people rolling fatefully down the smooth channel of history, everyone mingling, all of them tracing a common lineage back and back to a discrete ancestor. It wasn’t. Our river of time looked more like this, a braided stream:

i-509a6173b32bf82c2719f4b31f1f1aa3-braided.jpeg

This is what we mean when we talk about populations having structure. Branches emerge, whether we call them Neandertals or Denisovans or modern humans, and they are distinct but there can still be genes flowing between them to some degree. Even within modern humans we have structure, where groups maintain a kind of genetic integrity over space and time; I can look at my own recent lineage and see how my mother’s Scandinavian connections were maintained through several generations in America, or I can look at my father’s pedigree that goes back about 400 years in the New World and see that even though they were constantly scudding along at the very edge of the American frontier, mingling with Native Americans and black slaves and freedmen and Chinese railroad workers and Japanese farmers, somehow in their marriages, nothing but Scots/Irish/Anglo-Saxon names turn up.

That’s the nature of a species: many channels, many populations, not just one, separating and merging with circumstance. It’s always been this way; when humans and chimps first diverged from their common ancestors, it wasn’t like one tribe went left, one went right, and they never talked to each other again — it was many streams of ancient ape populations twisted about amongst each other, gradually disentangling to each form a spectrum of divergent channels for each separated species.

When a creationist demands to see the “missing link”, it’s like looking at the picture of a river above and asking for the one drop of water that started it all. There wasn’t one. The question doesn’t even make sense. It’s why BioLogos looks so ridiculous when they worry over whether we can trace our ancestry back to two people, Adam and Eve — of course we can’t, humanity has never been represented by just two unique individuals, and even considering the issue seriously reveals an absence of understanding of how populations evolve. It’s so confused, it’s not even wrong.

(I notice that Greg Laden comes to a similar conclusion, that using the term “missing link” should be avoided, but the nature of his argument looks about as tangled and discursive as the picture of the braided stream above…so maybe it’s more true to the reality?)

How to afford a big sloppy genome

i-e88a953e59c2ce6c5e2ac4568c7f0c36-rb.png

My direct experience with prokaryotes is sadly limited — while our entire lives and environment are profoundly shaped by the activity of bacteria, we rarely actually see the little guys. The closest I’ve come was some years ago, when I was doing work on grasshopper embryos, and sterile technique was a pressing concern. The work was done under a hood that we regularly hosed down with 95% alcohol, we’d extract embryos from their eggs, and we’d keep them alive for hours to days in tissue culture medium — a rich soup of nutrients that was also a ripe environment for bacterial growth. I was looking at the development of neurons, so I’d put the embryo under a high-powered lens of a microscope equipped with differential interference contrast optics, and the sheet of grasshopper neurons would look like a giant’s causeway, a field of tightly packed rounded boulders. I was watching processes emerging and growing from the cells, so I needed good crisp optics and a specimen that would thrive healthily for a good long period of time.

It was a bad sign when bacteria would begin to grow in the embryo. They were visible like grains of rice among the ripe watermelons of the cells I was interested in, and when I spotted them I knew my viewing time was limited: they didn’t obscure much directly, but soon enough the medium would be getting cloudy and worse, grasshopper hemocytes (their immune cells) would emerge and do their amoeboid oozing all over the field, engulfing the nasty bacteria but also obscuring my view.

What was striking, though, was the disparity in size. Prokaryotic bacteria are tiny, so small they nestled in the little nooks between the hopper cells; it was like the opening to Star Wars, with the tiny little rebel corvette dwarfed by the massive eukaryotic embryonic cells that loomed vastly in the microscope, like the imperial star destroyer that just kept coming and totally overbearing the smaller targets. And the totality of the embryo itself — that’s no moon. It’s a multicellular organism.

I had to wonder: why have eukaryotes grown so large relative to their prokaryotic cousins, and why haven’t any prokaryotes followed the strategy of multicellularity to build even bigger assemblages? There is a pat answer, of course: it’s because prokaryotes already have the most successful evolutionary strategy of them all and are busily being the best microorganisms they can be. Evolving into a worm would be a step down for them.

That answer doesn’t work, though. Prokaryotes are the most numerous, most diverse, most widely successful organisms on the planet: in all those teeming swarms and multitudinous opportunities, none have exploited this path? I can understand that they’d be rare, but nonexistent? The only big multicellular organisms are all eukaryotic? Why?

Another issue is that it’s not as if eukaryotes carry around fundamentally different processes: every key innovation that allowed multicellularity to occur was first pioneered in prokaryotes. Cell signaling? Prokaryotes have it. Gene regulation? Prokaryotes have that covered. Functional partitioning of specialized regions of the cell? Common in prokaryotes. Introns, exons, endocytosis, cytoskeletons…yep, prokaryotes had it first, eukaryotes have simply elaborated upon them. It’s like finding a remote tribe that has mastered all the individual skills of carpentry — nails and hammers, screws and screwdrivers, saws and lumber — as well as plumbing and electricity, but no one has ever managed to bring all the skills together to build a house.

Nick Lane and William Martin have a hypothesis, and it’s an interesting one that I hadn’t considered before: it’s the horsepower. Eukaryotes have a key innovation that permits the expansion of genome complexity, and it’s the mitochondrion. Without that big powerplant, and most importantly, a dedicated control mechanism, prokaryotes can’t afford to become more complex, so they’ve instead evolved to dominate the small, fast, efficient niche, leaving the eukaryotes to occupy the grandly inefficient, elaborate sloppy niche.

Lane and Martin make their case with numbers. What is the energy budget for cells? Somewhat surprisingly, even during periods of rapid growth, bacteria sink only about 20% of their metabolic activity into DNA replication; the costly process is protein synthesis, which eats up about 75% of the energy budget. It’s not so much having a lot of genes in the genome that is expensive, it’s translating those genes into useful protein products that costs. And if a bacterium with 4400 genes is spending that much making them work, it doesn’t have a lot of latitude to expand the number of genes — double them and the cell goes bankrupt. Yet eukaryotic cells can have ten times that number of genes.

Another way to look at it is to calculate the metabolic output of the typical cell. A culture of bacteria may have a mean metabolic rate of 0.2 watts/gram; each cell is tiny, with a mass of 2.6 x 10-12g, which means each cell is producing about 0.5 picowatts. A eukaryotic protist has about the same power output per unit weight, 0.06 watts/gram, but each cell is so much larger, about 40,000 x 10-12g, that a single cell has about 2300 picowatts available to it. So, more energy!

Now the question is how that relates to genome size. If the prokaryote has a genome that’s about 6 megabases long, that means it has about 0.08 picowatts/megabase to spare. If the eukaryote genome is 3,000 megabytes long, that translates into about 0.8 picowatts of power per megabase (that’s a tenfold increase, but keep in mind that there is wide variation in size in both prokaryotes and eukaryotes, so the ranges overlap and we can’t actually consider this a significant difference — they’re in the same ballpark).

Now you should be thinking…this is just a consequence of scaling. Eukaryotic power production per gram isn’t any better than what prokaryotes do, all they’ve done is made their cells bigger, and there’s nothing to stop prokaryotes from growing large and doing the same thing. In fact, they do: the largest known bacterium, Thiomargarita, can reach a diameter of a half-millimeter. It gets more metabolic power in a similar way to how eukaryotes do it: we eukaryotes carry a population of mitochondria with convoluted membranes and a dedicated strand of DNA, all to produce energy, and the larger the cell, the more mitochondria are present. Thiomargarita doesn’t have mitochondria, but it instead duplicates its own genome many times over, with 6,000-17,000 nucleoids distributed around the cell, each regulating its own patch of energy-producing membrane. It’s functionally equivalent to the eukaryotic mitochondrial array then, right?

Wrong. There’s a catch. Mitochondria have grossly stripped down genomes, carrying just a small cluster of genes essential for ATP production. One hypothesis for why this mitochondrial genome is maintained is that it acts as a local control module, rapidly responding to changes in the local membrane to regulate the structure. In Thiomargarita, in order to get this fine-tuned local control, the whole genome is replicated, dragging along all the baggage, and metabolic expense, of all of those non-metabolic genes.

Because it is amplifying the entire genomic package instead of just an essential metabolic subset, Thiomargarita‘s energy output per gene plummets in comparison. That difference is highlighted in this illustration which compares an ‘average’ prokaryote, Escherichia, to a giant prokaryote, Thiomargarita, to an ‘average’ eukaryotic protist, Euglena.

i-3ec4f5c02d3305d25182f69119307702-cellpower-thumb-400x336-59593.jpeg
(Click for larger image)
The cellular power struggle. a-c, Schematic representations of a medium sized prokaryote (Escherichia), a very large prokaryote (Thiomargarita), and a medium-sized eukaryote (Euglena). Bioenergetic membranes across which chemiosmotic potential is generated and harnessed are drawn in red and indicated with a black arrow; DNA is indicated in blue. In c, the mitochondrion is enlarged in the inset, mitochondrial DNA and nuclear DNA are indicated with open arrows. d-f, Power production of the cells shown in relation to fresh weight (d), per haploid gene (e) and per haploid genome (power per haploid gene times haploid gene number) (f). Note that the presence or absence of a nuclear membrane in eukaryotes, although arguably a consequence of mitochondrial origin70, has no impact on energetics, but that the energy per gene provided by mitochondria underpins the origin of the genomic complexity required to evolve such eukaryote-specific traits.

Notice that the prokaryotes are at no disadvantage in terms of raw power output; eukaryotes have not evolved bigger, better engines. Where they differ greatly is in the amount of power produced per gene or per genome. Eukaryotes are profligate in pouring energy into their genomes, which is how they can afford to be so disgracefully inefficient, with numerous genes with only subtle differences between them, and with large quantities of junk DNA (which is also not so costly anyway; remember, the bulk of the expense is in translating, not replicating, the genome, and junk DNA is mostly untranscribed).

So, what Lane and Martin argue is that the segregation of energy production into functional modules with an independent and minimal genetic control mechanism, mitochondria with mitochondrial DNA, was the essential precursor to the evolution of multicellular complexity — it’s what gave the cell the energy surplus to expand the genome and explore large-scale innovation.

As they explain it…

Our considerations reveal why the exploration of protein sequence space en route to eukaryotic complexity required mitochondria. Without mitochondria, prokaryotes—even giant polyploids—cannot pay the energetic price of complexity; the lack of true intermediates in the prokaryote-to-eukaryote transition has a bioenergetic cause. The conversion from endosymbiont to mitochondrion provided a freely expandable surface area of internal bioenergetic membranes, serviced by thousands of tiny specialized genomes that permitted their host to evolve, explore and express massive numbers of new proteins in combinations and at levels energetically unattainable for its prokaryotic contemporaries. If evolution works like a tinkerer, evolution with mitochondria works like a corps of engineers.

That last word is unfortunate, because they really aren’t saying that mitochondria engineer evolutionary change at all. What they are is permissive: they generate the extra energy that allows the nuclear genome the luxury of exploring a wider space of complexity and possible solutions to novel problems. Prokaryotes are all about efficiency and refinement, while eukaryotes are all about flamboyant experimentation by chance, not design.

Lane N, Martin W. (2010) The energetics of genome complexity. Nature 467(7318):929-34.